Electric field interactions in pairs of electric fish: modeling and mimicking naturalistic inputs

Weakly electric fish acquire information about their surroundings by detecting and interpreting the spatial and temporal patterns of electric potential across their skin, caused by perturbations in a self-generated, oscillating electric field. Computational and experimental studies have focused on understanding the electric images due to simple, passive objects. The present study considers electric images of a conspecific fish. It is known that the electric fields of two fish interact to produce beats with spatially varying profiles of amplitude and phase. Such patterns have been shown to be critical for electrosensory-mediated behaviours, such as the jamming avoidance response, but they have yet to be well described. We have created a biophysically realistic model of a wave-type weakly electric fish by using a genetic algorithm to calibrate the parameters to the electric field of a real fish. We use the model to study a pair of fish and compute the electric images of one fish onto the other at three representative phases within a beat cycle. Analysis of the images reveals rostral/caudal and ipsilateral/contralateral patterns of amplitude and phase that have implications for localization of conspecifics (both position and orientation) and communication between conspecifics. We then show how the common stimulation paradigm used to mimic a conspecific during in vivo electrophysiological experiments, based on a transverse arrangement of two electrodes, can be improved in order to more accurately reflect the important qualitative features of naturalistic inputs, as revealed by our model.     

Differential responses of two types of electroreceptive afferents to signal distortions may permit capacitance measurement in a weakly electric fish,Gnathonemus petersii

Summary Gnathonemus petersii discriminates between ohmic and capacitive objects. To investigate the sensory basis of this discrimination we recorded from primary afférents that innervate either A or B mormyromast sensory cells. Modified and natural electric organ discharges were used as stimuli. In both A and B fibres frequencies below the peak-power frequency (3.8 to 4.5 kHz) of the electric organ discharge caused minimal first-spike latencies and a maximum number of spikes. A fibres did not discriminate phase-shifted stimuli, whereas B fibres responded significantly with a decrease in first-spike latency if the phase shift was only — 1°. In both A and B fibres an amplitude increase caused a decrease in spike latency and an increase in spike number; an amplitude decrease had the reverse effect. If stimulated with quasi-natural electric organ discharges distorted by capacitive objects, the responses of A fibres decreased with increasing signal distortion. In contrast, the responses of B fibres increased until amplitude effects began to dominate. Gnathonemus may use the physiological differences between A and B fibres to detect and discriminate between capacitive and purely ohmic objects.Abbreviations ELL electrosensory lateral line lobe - EOD electric organ discharge - LFS local filtered signal - p-p peak-to-peak     

Neuronal control of behavioral plasticity: the prepacemaker nucleus of weakly electric gymnotiform fish

 Gymnotiform fish of the genera Apteronotus and Eigenmannia provide an excellent vertebrate model system to study neural mechanisms controlling behavioral plasticity. These teleosts generate, by means of an electric organ, quasi-sinusoidal discharges of extremely stable frequency and waveform. Modulations consisting of transient rises in discharge frequency are produced during social encounters, and play an important role in communication. These so-called “chirps” exhibit a remarkable sexual dimorphism, as well as an enormous seasonal and individual variability. Chirping behavior is controlled by a subset of neurons in the complex of the central posterior/prepacemaker nucleus in the diencephalon. It is hypothesized that the plasticity in the performance of chirping behavior is, at least in part, governed by two mechanisms: first, by seasonally induced structural changes in dendritic morphology of neurons of the prepacemaker nucleus, thus leading to pronounced alterations in excitatory input. Second, by androgen-controlled changes in the innervation pattern of the prepacemaker nucleus by fibers expressing the neuropeptide substance P. In addition to these two dynamic processes, cells are generated continuously and at high number in the central posterior/prepacemaker nucleus during adulthood. This phenomenon may provide the basis for a “refreshment”, thus facilitating possible changes in the underlying neural network. Accepted: 17 September 1990     

Mauthner cell-evoked synaptic actions on pacemaker medullary neurons of a weakly electric fish

The present study was designed to examine the synaptic events in neurons of the pacemaker nucleus of Gymnotus carapo during the increase in rate of the electric organ discharge following activation of Mauthner cells. Pacemaker and relay cells were investigated using intracellular recordings which were performed under two different conditions: (1) with the pacemaker nucleus spontaneously discharging and (2) after its activity was abolished by anesthesia. Mauthner axon activation induced an increase in the rate of pacemaker cell discharges. This response was accompanied by an increase in the slope of the pacemaker potential (up to 110%) and a depolarization of these cells. The discharges of relay cells followed one to one those of pacemaker cells. In contrast to that observed in pacemaker cells, only brief depolarizing antidromic effects could be evoked in relay cells after Mauthner axon activation. In quiescent pacemaker cells, Mauthner cell activation induced a prolonged (up to 500 ms) depolarizing potential with an average amplitude of 1.92 ± 0.82 mV; its latency was 4.43 ± 1.14 ms. Our data indicate that, within the pacemaker nucleus, the population of pacemaker cells is the only target for Mauthner cell-evoked, short-latency excitatory synaptic actions. Accepted: 1 March 1997     

Discrimination of objects through electrolocation in the weakly electric fish,Gnathonemus petersii

Summary Three weakly electric fish (Gnathonemus petersii) were force-choice trained in a two-alternative procedure to discriminate between objects differing in their electrical characteristics. The objects were carbon dipoles in plexiglass tubing (length 2.5 cm, diameter 0.6 cm). Their electrical characteristics could be changed by varying the impedance of an external circuit to which they were connected (Fig. 1). In one (the capacitance dipole) the resistance was very low(< 3 ) and the capcitance variable. In the other (the resistance dipole) the resistance was variable and the capacitance low (<50 pF).Capacitances from several hundred pF (lower thresholds, Fig. 2) to several hundred nF (upper thresholds, Fig. 3) could be discriminated from both insulators and good conductors. In all cases the reward-negative stimulus was the capacitance dipole, which was avoided by all fish spontaneously. Thresholds were defined at 70% correct choices.The fish were then tested for their ability to discriminate between one object with a given capacitance and another with resistances varying from 3 to 200 k. The capacitance dipole continued to be the negative stimulus throughout. All 3 fish avoided it in at least 80% of the trials at each stimulus combination (Fig. 4). This result suggests that Gnathonemus perceives the capacitance and the resistance of objects differentially.The effect of the dipole-objects as well as some natural objects on the local EOD was recorded differentially very close to the fish's skin (Fig. 5). The amplitude of the local EODs was affected by all types of objects as they approached the skin. However, the waveform was changed only by capacitance dipoles and some natural objects (Figs. 6 and 7). It appears that the fish perceive not only intensity changes in the local EOD but wave-form deformations as well and can thus distinguish objects of different complex impedances.Abbreviations EOD electric organ discharge - f _max maximal spectral frequency - GP Gnathonemus petersii - LFS local filtered signal - PMA probing motor act - S+ positive stimulus - S negative stimulus     

Ontogeny of the electric organ discharge and the electric organ in the weakly electric pulse fish Brachyhypopomus pinnicaudatus (Hypopomidae, Gymnotiformes)

I recorded the electric organ discharges (EODs) of 331 immature Brachyhypopomus pinnicaudatus 6–88 mm long. Larvae produced head-positive pulses 1.3 ms long at 7 mm (6 days) and added a second, small head-negative phase at 12 mm. Both phases shortened duration and increased amplitude during growth. Relative to the whole EOD, the negative phase increased duration until 22 mm and amplitude until 37 mm. Fish above 37 mm produced a “symmetric” EOD like that of adult females. I stained cleared fish with Sudan black, or fluorescently labeled serial sections with anti-desmin (electric organ) or anti-myosin (muscle). From day 6 onward, a single electric organ was found at the ventral margin of the hypaxial muscle. Electrocytes were initially cylindrical, overlapping, and stalk-less, but later shortened along the rostrocaudal axis, separated into rows, and formed caudal stalks. This differentiation started in the posterior electric organ in 12-mm fish and was complete in the anterior region of fish with “symmetric” EODs. The lack of a distinct “larval” electric organ in this pulse-type species weakens the hypothesis that all gymnotiforms develop both a temporary (larval) and a permanent (adult) electric organ. Accepted: 1 March 1997     

Adaptive processing in electrosensory systems: Links to cerebellar plasticity and learning

The first central stage of electrosensory processing in fish takes place in structures with local circuitry that resembles the cerebellum. Cerebellum-like structures and the cerebellum itself share common patterns of gene expression and may also share developmental and evolutionary origins. Given these similarities it is natural to ask whether insights gleaned from the study of cerebellum-like structures might be useful for understanding aspects of cerebellar function and vice versa. Work from electrosensory systems has shown that cerebellum-like circuitry acts to generate learned predictions about the sensory consequences of the animals’ own behavior through a process of associative plasticity at parallel fiber synapses. Subtraction of these predictions from the actual sensory input serves to highlight unexpected and hence behaviorally relevant features. Learning and prediction are also central to many current ideas regarding the function of the cerebellum itself. The present review draws comparisons between cerebellum-like structures and the cerebellum focusing on the properties and sites of synaptic plasticity in these structures and on connections between plasticity and learning. Examples are drawn mainly from the electrosensory lobe (ELL) of mormyrid fish and from extensive work characterizing the role of the cerebellum in Pavlovian eyelid conditioning and vestibulo-ocular reflex (VOR) modification. Parallels with other cerebellum-like structures, including the gymnotid ELL, the elasmobranch dorsal octavolateral nucleus (DON), and the mammalian dorsal cochlear nucleus (DCN) are also discussed.     

The electric image in weakly electric fish: I. A data-based model of waveform generation inGymnotus carapo

Understanding how electrosensory images are generated and perceived in actively electrolocating fish requires the study of the characteristics of fish bodies as electric sources. This paper presents a model ofGymnotus carapo based on measurements of the electromotive force generated by the electric organ and the impedance of the passive tissues. A good agreement between simulated and experimentally recorded transcutaneous currents was obtained. Passive structures participate in the transformation of the electromotive force pattern into transcutaneous current profiles. These spatial filtering properties of the fish's body were investigated using the model. The shape of the transcutaneous current profiles depends on tissue resistance and on the geometry and size of the fish. Skin impedance was mainly resistive. The effect of skin resistance on the spatial filtering properties of the fish's body was theoretically analyzed.The model results show that generators in the abdominal and central regions produce most of the currents through the head. This suggests that the electric organ discharge (EOD), generated in the abdominal and central regions is critical for active electrolocation. In addition, the well-synchronized EOD components generated all along the fish produce large potentials in the far field. These components are probably involved in long-distance electrocommunication.Preliminary results of this work were published as a symposium abstract.     

Time coding in the midbrain of mormyrid electric fish. II. Stimulus selectivity in the nucleus exterolateralis pars posterior

The anterior and posterior exterolateral nuclei (ELa and ELp) of the mormyrid midbrain are thought to play a critical role in the temporal analysis of the electric discharge waveforms of other individuals. The peripheral electroreceptors receiving electric organ discharges (EODs) of other fish project through the brainstem to ELa via a rapid conducting pathway. EODs, composed of brief, but stereotyped waveforms are encoded as a temporal pattern of spikes. From previous work, we know that phase locking is precise in ELa. Here it is shown that evoked potentials recorded from ELp show a similar high degree of phase locking, although the evoked potentials last much longer. Single-unit recordings in ELp reveal two distinct populations of neurons in ELp: type I cells are responsive to voltage step functions, and not tuned for stimulus duration; type II cells are tuned to a specific range of stimulus durations. Type II cells are less responsive than type I cells, tend to respond with bursts of action potentials rather than with single spikes, have a longer latency, show weaker time locking to stimuli, and are more sensitive to stimulus polarity and amplitude. The stimulus selectivity of type II cells may arise from convergence of type I cell inputs. Despite the loss of rapid conduction between ELa and ELp, analysis of temporal features of waveforms evidently continues in ELp, perhaps through a system of labeled lines. Accepted: 25 June 1997     

Responses of cells in the mormyrid electrosensory lobe to EODs with distorted waveforms: implications for capacitance detection

Mormyrid fish (Gnathonemus petersii) can discriminate between ohmic and capacitive electrical objects during active electrolocation. The neural basis of this ability was investigated by recording cells in the dorsolateraland medial zones of the electrosensory lobe. Natural electric organ discharges (EODs) distorted by capacitive objects and EODs with computer generated phase shifts were used as stimuli.Cells in the dorsolateral zone were very sensitive to phase shifted EODs with constant amplitude spectra. Phase shifts as small as 1 were effective. Cells in this zone also responded more to EODs with capacitance induced distortions than to non-distorted EODs. These effects were very similar to the effects on B-type primary afferents from mormyromast electroreceptors which project to this zone.Cells in the medial zone were not sensitive to phase shifted EODs. Capacitance induced waveform distortions were effective, but the effect of such distortions was opposite to the effect on dorsolateral zone cells. These effects were very similar to the effects on A-type primary afferents from mormyromast electroreceptors which project to this zone.The results show that peripheral information about capacitive objects is preserved in the electrosensory lobe, but do not indicate any further processing of capacitive information in the lobe.     

Ionic currents that contribute to a sexually dimorphic communication signal in weakly electric fish

Weakly electric fish produce a communication signal, the electric organ discharge, that is species specific, and in many species, sexually dimorphic. Because the neural circuit that controls the electric organ discharge is relatively simple, it is an excellent model in which to study both the biophysical mechanisms underlying a rhythmic behavior and the neuroendocrine control of a sexually dimorphic behavior. By studying the effects of ion channel blockers on neurons in the medullary pacemaker nucleus, I pharmacologically characterized three ionic currents that influence the pacemaker rhythm, and thus electric organ discharge frequency, in the gymnotiform fish, Apteronotus leptorhynchus. These currents included a tetrodotoxin-sensitive sodium current; a potassium current that was sensitive to 4-aminopyridine; and a calcium current that was sensitive to nickel and cadmium, but resistant to specific blockers of L-, N-, P-, and Q-type calcium currents. The pharmacological profiles of the ionic currents in the pacemaker nucleus are similar to those of ionic currents involved in pacemaking in other neuronal oscillators. Because these ionic currents dramatically influence pacemaker firing frequency, which is directly related to electric organ discharge frequency, these ionic currents are likely targets of steroid hormone action in producing sexual dimorphisms in electric organ discharge frequency. Additional studies are needed to determine how these ionic currents interact to generate the electric organ discharge rhythm and to investigate the possibility that sexual dimorphism in the electric organ discharge results from the actions of gonadal steroids on these ionic currents. Accepted: 3 June 1999     

Characterization and modeling of P-type electrosensory afferent responses to amplitude modulations in a wave-type electric fish

The first stage of information processing in the electrosensory system involves the encoding of local changes in transdermal potential into trains of action potentials in primary electrosensory afferent nerve fibers. To develop a quantitative model of this encoding process for P-type (probability-coding) afferent fibers in the weakly electric fish Apteronotus leptorhynchus, we recorded single unit activity from electrosensory afferent axons in the posterior branch of the anterior lateral line nerve and analyzed responses to electronically generated sinusoidal amplitude modulations of the local transdermal potential. Over a range of AM frequencies from 0.1 to 200 Hz, the modulation transfer function of P-type afferents is high-pass in character, with a gain that increases monotonically up to AM frequencies of 100 Hz where it begins to roll off, and a phase advance with a range of 15–60 degrees. Based on quantitative analysis of the observed gain and phase characteristics, we present a computationally efficient model of P-type afferent response dynamics which accurately characterizes changes in afferent firing rate in response to amplitude modulations of the fish's own electric organ discharge over a wide range of AM frequencies relevant to active electrolocation. Accepted: 14 June 1997     

Responses of neurons in the electrosensory lateral line lobe of the weakly electric fish <Emphasis Type="Italic">Gnathonemus petersii</Emphasis> to simple and complex electrosensory stimuli

Mormyrid fish use active electrolocation to detect and analyze objects. The electrosensory lateral line lobe in the brain receives input from electroreceptors and an efference copy of the command to discharge the electric organ. In curarized fish, we recorded extracellularly from neurons of the electrosensory lateral line lobe while stimulating in the periphery with either a local point stimulus or with a more natural whole-body stimulus. Two classes of neurons were found: (1) three types of E-cells, which were excited by a point stimulus; and (2) two types of I-cells, which were inhibited by point stimulus and responded with excitation to the electric organ corollary discharge. While all neurons responded to a point stimulus, only one out of two types of I-units and two of the three types of E-units changed their firing behavior to a whole-body stimulus or when an object was present. In most units, the responses to whole-body stimuli and to point stimuli differed substantially. Many electrosensory lateral line lobe units showed neural plasticity after prolonged sensory stimulation. However, plastic effects during whole body stimulation were often unlike those occurring during point stimuli, suggesting that under natural conditions electrosensory lateral line lobe network effects play an important role in shaping neural plasticity.     

Adaptive radiation in African weakly electric fish (Teleostei: Mormyridae: Campylomormyrus): a combined molecular and morphological approach

We combined multiple molecular markers and geometric morphometrics to revise the current taxonomy and to build a phylogenetic hypothesis for the African weakly electric fish genus Campylomormyrus. Genetic data (2039 bp DNA sequence of mitochondrial cytochrome b and nuclear S7 genes) on 106 specimens support the existence of at least six species occurring in sympatry. We were able to further confirm these species by microsatellite analysis at 16 unlinked nuclear loci and landmark-based morphometrics. We assigned them to nominal taxa by comparisons to type specimens of all Campylomormyrus species recognized so far. Additionally, we showed that the shape of the elongated trunk-like snout is the major source of morphological differentiation among them. This finding suggests that the radiation of this speciose genus might have been driven by adaptation to different food sources.     

Life-history plasticity under resource stress in a clonal fish (Poeciliidae: Poeciliopsis)

Within-individual plasticity for reproductive investment was examined in a clonal fish (Poeciliidae: Poeciliopsis) grown under six levels of resource stress. Growth, age at first reproduction, egg production, egg size, egg energetic content, and survivorship were measured from fish grown in three dietary and two density treatments. Growth and fecundity decreased with both increased density and food stress. Age at first reproduction increased with increased density, but was unaffected by the diet treatments. Reproductive effort (clutch size per female weight), offspring investment (egg size and egg energetic content), and survivorship were invariant across all treatment combinations. We compare these results with predictions based on theoretical treatments of optimal reproductive investment.     

Calcium dynamics in dendritic spines: a link to structural plasticity

Calcium signals evoked either by action potential or by synaptic activity play a crucial role for the synaptic plasticity within an individual spine. Because of the small size of spine and the indicators commonly used to measure spine calcium activity, calcium function can be severely disrupted. Therefore, it is very difficult to explain the exact relationship between spine geometry and spine calcium dynamics. Recently, it has been suggested that the medium range of calcium which induces long term potentiation leads to the structural stability stage of spines, while very low or very high amount of calcium leads to the long term depression stage which results in shortening and eventually pruning of spines. Here we propose a physiologically realistic computational model to examine the role of calcium and the mechanisms that govern its regulation in the spine morphology. Calcium enters into spine head through NMDA and AMPA channels and is regulated by internal stores. Contribution of this calcium in the induction of long term potentiation and long term depression is also discussed. Further it has also been predicted that the presence of internal stores depletes the total calcium accumulation in cytosol which is in agreement with the recent experimental and theoretical studies.     

Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish

Determining the capacity of organisms to acclimate and adapt to increased temperatures is key to understand how populations and communities will respond to global warming. Although there is evidence that elevated water temperature affects metabolism, growth and condition of tropical marine fish, it is unknown whether they have the potential to acclimate, given adequate time. We reared the tropical reef fish Acanthochromis polyacanthus through its entire life cycle at present day and elevated (+1.5 and+3.0 °C) water temperatures to test its ability to thermally acclimate to ocean temperatures predicted to occur over the next 50–100 years. Fish reared at 3.0 °C greater than the present day average reduced their resting oxygen consumption (RMR) during summer compared with fish reared at present day temperatures and tested at the elevated temperature. The reduction in RMR of up to 69 mg O₂ kg^?1 h^?1 in acclimated fish could represent a significant benefit to daily energy expenditure. In contrast, there was no acclimation to summer temperatures exhibited by fish reared at 1.5 °C above present day temperatures. Fish acclimated to +3.0 °C were smaller and in poorer condition than fish reared at present day temperatures, suggesting that even with acclimation there will be significant consequences for future populations of tropical fishes caused by global warming.     

Hormonal and body size correlates of electrocommunication behavior during dyadic interactions in a weakly electric fish, Apteronotus leptorhynchus

Brown ghost knife fish, Apteronotus leptorhynchus, produce sexually dimorphic, androgen-sensitive electrocommunication signals termed chirps. The androgen regulation of chirping has been studied previously by administering exogenous androgens to females and measuring the chirping response to artificial electrical signals. The present study examined the production of chirps during dyadic interactions of fish and correlated chirp rate with endogenous levels of one particular androgen, 11-ketotestosterone (11KT). Eight males and four females were exposed to short-term (5-min) interactions in both same-sex and opposite-sex dyads. Twenty-four hours after all behavioral tests, fish were bled for determination of plasma 11KT levels. Males and females differed in both their production of chirps and their ability to elicit chirps from other fish: males chirped about 20-30 times more often than females and elicited 2-4 times as many chirps as females. Among males, chirp rate was correlated positively with plasma 11KT, electric organ discharge frequency, and body size. Combined with results from experimental manipulation of androgen levels, these results support the hypothesis that endogenous 11KT levels influence electrocommunication behavior during interactions between two male fish.     

Differentiation of morphology, genetics and electric signals in a region of sympatry between sister species of African electric fish (Mormyridae)

Mormyrid fishes produce and sense weak electric organ discharges (EODs) for object detection and communication, and they have been increasingly recognized as useful model organisms for studying signal evolution and speciation. EOD waveform variation can provide important clues to sympatric species boundaries between otherwise similar or morphologically cryptic forms. Endemic to the watersheds of Gabon (Central Africa), Ivindomyrus marchei and Ivindomyrus opdenboschi are morphologically similar to one another. Using morphometric, electrophysiological and molecular characters [cytochrome b sequences and amplified fragment length polymorphism (AFLP) genotypes], we investigated to what extent these nominal mormyrid species have diverged into biological species. Our sampling covered the known distribution of each species with a focus on the Ivindo River, where the two taxa co-occur. An overall pattern of congruence among datasets suggests that I. opdenboschi and I. marchei are mostly distinct. Electric signal analysis showed that EODs of I. opdenboschi tend to have a smaller initial head-positive peak than those of I. marchei, and they often possess a small third waveform peak that is typically absent in EODs of I. marchei. Analysis of sympatric I. opdenboschi and I. marchei populations revealed slight, but significant, genetic partitioning between populations based on AFLP data (F(ST) approximately 0.04). Taken separately, however, none of the characters we evaluated allowed us to discriminate two completely distinct or monophyletic groups. Lack of robust separation on the basis of any single character set may be a consequence of incomplete lineage sorting due to recent ancestry and/or introgressive hybridization. Incongruence between genetic datasets in one individual, which exhibited a mitochondrial haplotype characteristic of I. marchei but nevertheless fell within a genetic cluster of I. opdenboschi based on AFLP genotypes, suggests that a low level of recent hybridization may also be contributing to patterns of character variation in sympatry. Nevertheless, despite less than perfect separability based on any one dataset and inconclusive evidence for complete reproductive isolation between them in the Ivindo River, we find sufficient evidence to support the existence of two distinctive species, I. opdenboschi and I. marchei, even if not 'biological species' in the Mayrian sense.